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Zeitschrift/Journal: Herpetozoa

Jahr/Year: 2019

Band/Volume: 31_3_4

Autor(en)/Author(s): Stümpel Nikolaus, Zinenko Oleksander, Mebert Konrad

Artikel/Article: on elevation-related shifts of spring activity in male vipers of the genera and Macrovipera in and 125-132 StuempelZinenkoMebert_Spring_activity_Montivipera-Macrovipera:HERPETOZOA.qxd 12.02.2019 15:04 Seite 1

HERPEToZoA 31 (3/4): 125 - 132 125 Wien, 28. Februar 2019

on elevation-related shifts of spring activity in male vipers of the genera Montivipera and Macrovipera in Turkey and Cyprus (: serpentes: )

Zur höhenabhängigen Frühjahrsaktivität männlicher Vipern der Gattungen Montivipera und Macrovipera in der Türkei und Zypern (squamata: serpentes: Viperidae)

NikolAus sTüMPEl & o lEksANdR ZiNENko & k oNRAd MEbERT

kuRZFAssuNG der zeitliche Ablauf von lebenszyklen wechselwarmer Wirbeltiere wird in hohem Maße vom Temperaturregime des lebensraumes bestimmt. in Gebirgen sinkt die umgebungstemperatur mit zunehmender Höhenlage. deshalb liegt es nahe, anzunehmen, daß die Höhenlage den Zeitpunkt des beginns der Frühjahres- aktivität von Vipern beeinflußt. um diesen Zusammenhang zu untersuchen, haben die Autoren im Zeitraum von 2004 bis 2015 in der Türkei und auf Zypern den beginn der Frühjahrshäutung bei männlichen Vipern der Gattun- gen Montivipera und Macrovipera zwischen Meereshöhe und 2300 m ü. M. untersucht. sexuell aktive Männchen durchlaufen nach der Winterruhe und vor der Paarung eine obligatorische Frühjahrshäutung. im Häutungsprozeß werden äußerlich klar differenzierbare stadien durchschritten, von denen die Eintrübung des Auges besonders auffällig und kurzzeitig ist. dieses stadium ist daher prädestiniert, um den nachwinterlichen Aktivitätsbeginn zwischen Populationen unterschiedlicher Höhenlagen miteinander zu verglei - chen. Während der Freilandstudien wurden insgesamt 15 adulte männliche Vipern mit milchig-opaken Augen angetroffen, welche ihren Häutungsstatus anzeigten. die vorliegenden Ergebnisse zeigen einen signifikanten positiven Zusammenhang zwischen dem beginn der Frühjahreshäutung der untersuchten Vipern und der Höhenlage ihres Fundortes. Je höher der lebensraum lag, desto später im Jahr setzte die Frühjahrshäutung der Männchen ein. diese Ergebnisse können helfen, für die unter - suchten Arten die dauer der überwinterungsperiode in Abhängigkeit von der Höhenlage ihres Vorkommens abzu - schätzen. Nach bestem Wissen der Autoren ist die vorliegende studie die erste untersuchung, die einen Zusammenhang zwischen der Phänologie und der Höhenverbreitung bei eurasischen Vipern aufzeigt. AbsTRACT At a local scale, the timing of periodic life-history events of ectothermic vertebrates is strongly influenced by the ambient temperature. in the mountains, temperature decreases with increasing elevation. This is why the onset of spring activity of vipers can be expected to vary regionally between warm lowland and cold montane climates. To analyze the relationship between elevation and onset of spring activity, the authors surveyed habitats for emerg - ing male vipers of the genera Montivipera and Macrovipera between April and May in Turkey and Cyprus. sexually active male vipers shed soon after leaving their hibernacula and before mating. The male spring shedding is obligatory and therefore represents a chronometer for the onset of the vipers’ surface activity. during field trips between 2004 and 2015, fifteen male vipers were found in habitats between sea level and 2,300 m a.s.l. elevation with milky-opaque eyes reflecting their state of pre-ecdysis. The observed significant positive correlation between onset of the vipers’ spring activity and the elevation of the record site represents an ecological cline. The information can help to forecast duration of hibernation and activity of the vipers in the field. To the best knowledge of the authors, this is the first study about spring phenol - ogy of vipers from the eastern Mediterranean. kEY WoRds Reptilia: squamata: serpentes: Viperidae; Macrovipera lebetina , Montivipera bulgardaghica , Montivipera wagneri , , physiology, behavior, phenology, ecdysis, molting, spring shedding, activity, Turkey, Cyprus

iNTRoduCTioN

The ecosystems of the Near and viper out of three genera ( , harbor the highest diversity of Montivipera and Macrovipera ) are record - true vipers within Eurasia. Currently, 13 ed from the Turkish territory (e.g., NilsoN StuempelZinenkoMebert_Spring_activity_Montivipera-Macrovipera:HERPETOZOA.qxd 12.02.2019 15:04 Seite 2

126 N. s TüMPEl & o. Z iNENko & k. M EbERT

et al. 1988; sTüMPEl & J oGER 2009). With correlates with increased feeding, metabol - a few exceptions, the species within the ic rate and temperature ( sEMliTsCH 1979; genera are allopatrically distributed ( JoGER APPlEbY 1980; G ibsoN et al. 1989). it also 1984). Mountain Vipers, Montivipera spp., varies by reproductive state and cycle, and blunt-nosed Vipers, Macrovipera spp ., respectively, hormonal status, gender and were subjects to studies on zoogeography ontogenetic stage (e.g., kubiE et al. 1978; (JoGER 1984; M EbERT et al. 2016), taxono - NilsoN 1980; JACobsoN 2007; l illYWHiTE my ( NilsoN & A NdRéN 1986) and phylo- 2014 ). other influential factors may in - geny ( sTüMPEl & J oGER 2009; s TüMPEl et clude exposure to dry air and the resulting al. 2016). However, comparatively little is risk of increasing cutaneous evaporative known on their ecology (e.g ., N ilsoN et al. water loss ( lillYWHiTE & M AdERsoN 1982; 1999; ETTliNG et al. 2013, 2016), while MAdERsoN 1984; lillYWHiTE 2006), wear phenological data are completely lacking or and damage of the skin, as well as detach - hidden in grey literature. Macrovipera is ment of ectoparasites ( looMis 1951; HEAT- generally associated with -like to WolE 1999). semi-arid habitats situated between sea during ecdysis, histological process - level and 1,700 m a.s.l. and reaches its es, which occur in the epidermis, affect the western range limit in the Eastern Medi - external appearance of the gradually. terranean. species of the Monti - However, several stages of the process are vipera are found in a broader ecological very prominent and identifiable. The ecdy - and elevational spectrum. For example, in sis process lasts a minimum of 14 days in western and south-western Anatolia, these captivity (the authors’ personal observa - mountain vipers inhabit Mediterranean and tions) and is visually marked by a dull oromediterra nean biomes, whereas in east - appearance of the snake. Eight days prior ern Anatolia these vipers are associated to the actual skin shedding, the eyes turn with boreal and subalpine irano-Turanian visibly opaque (milky). This prominent floras. external change lasts for at least two days in ectothermic , climatic fac - under controlled lab conditions (the tors influence life history traits. Many of authors’ personal observations). Ecdysis them, such as seasonal and diurnal activity, culminates in the shedding of the old outer reproductive performance, growth rate and keratinized epithelial layer about six days metabolic rate depend on the thermal pro - after the eyes have become clear again (see files of the habitats (e.g., duVAll et al. MAdERsoN 1965). The entire process of 1985; VAN WYk 1995). Therefore, temper - skin renewal is influenced by environmen - ature is a relevant environmental factor to a tal factors (temperature, solar radiation) , defining part of its living space and and, e.g., can last about 40 days in Vipera shaping its abiotic components ( WAlkER et berus (l iNNAEus , 1798) at cool northern al. 1994; köRNER 1998; GREENlANd & latitudes (see olssoN et al. 1997), and like - los lEbEN 2001). Along with the increase ly is shorter in warmer regions or climate of elevation, also climatic, spatial, biotic zones. Furthermore, recent evidence from and evolutionary factors change ( MCCAiN the laboratory and field show that ecdysis & GRYTNEs 2010). The most obvious is the can be a synchronous process within snake generally linear decrease in temperature by populations, likely in correlation with envi - an average of approximately 0.68 °C per ronmental factors and/or pheromones, 100 m increase in elevation ( bARRY 2008). which influence physiology including Consequently, the seasonal and temporal reproductive cycles ( lilliWHiTE & s HEEHY activity of vipers inhabiting different eleva - iii 2016 and references therein). intra - tions can be expected to be affected by population synchrony of the first ecdysis extrinsic abiotic factors. following emergence from hibernacula was one such temporal activity is the observed in different snake groups in North shedding process in (ecdysis). in America (e.g., kubiE et al. 1978; FoRd general, ecdysis happens continuously 1996; P ARkER & ANdERsoN 2007) and throughout the lifetime and is associated places this synchronization into a seasonal with growth, whereby a higher frequency context. The pheromones released into the StuempelZinenkoMebert_Spring_activity_Montivipera-Macrovipera:HERPETOZOA.qxd 12.02.2019 15:04 Seite 3

on elevation-related shifts of spring activity in Montivipera and Macrovipera 127

environment during ecdysis inform other across a broad region, if the same stage of snakes in the area about the reproductive ecdysis is compared. Hence, milky eyes status of the newly shed snake ( kubiE et al. are an appropriate marker, as this stage is 1978; PARkER & M AsoN 2011). such a first the shortest and visually simplest to identi - annual (spring) ecdysis synchronization fy during ecdysis. that triggers mating activities has also been The authors hypothesize that the observed in the palearctic V. berus (sAiNT spring activity of vipers (including their GiRoNs 1980; and reviewed in NilsoN et al. reproductive behavior) is seasonally de - 2005). Female Aspic Vipers, Vipera aspis layed at high elevations in comparison to (l iNNAEus , 1758), shed their skin prior to lowland populations. The high amplitude ovulation, and ecdysis provides a reliable of the topographic relief of the eastern reference date for the onset of gestation Medi terranean and its exceptionally rich (loRioux et al. 2013). Hence, the release viper diversity provides a suitable opportu - of cutaneous pheromones plays an essential nity to analyze across taxa the association role in the reproductive behavior of temper - between the beginning of male spring activ - ate zone snakes, and thus, it is plausible that ity as indicated by the onset of ecdysis, and ecdysis coincides with the mating periods the elevation of occurrence. despite the (kubiE et al. 1978; MAsoN 1992; l illi- increasing amount of literature dealing with WHiTE & s HEEHY iii 2016). many aspects of seasonal and reproductive species of the genera Macrovipera behavior in snakes ( sHiNE 2003; AldRidGE and Montivipera belong to the “ berus ” & s EVER 2011; l illYWHiTE 2014), such a (NilsoN & A NdRéN 1997) with the spring correlation has not been subject to an obser - shedding of male vipers being the initiation vational study yet. of the reproductive activity (e.g., NilsoN The aim of the present study was to 1980; s AiNT GiRoNs 1980). Consequently, test the hypothesis that in adult male vipers the synchronized spring shedding can be of the genera Montivipera and Macrovipera used as a chronometer for phenology and the date of first ecdysis after hibernation is allows comparison of activity patterns of positively correlated with the elevation of populations from different elevations their occurrence in their natural habitat.

MATERiAls ANd METHods

data were gathered during eight field - bulgardaghica (NilsoN & A NdRéN , 1985)], trips to Turkey and Cyprus between 2004 dibek Mts. [ M. bulgardaghica albizona (Nil - and 2015. From March to May, potential soN , A NdREN & F läRdH , 1990)], and Aras habitats of four species of Montivipera and Valley in northeastern Turkey [ M. wagneri one of Macrovipera were surveyed to detect (N ilsoN & A NdRéN , 1984) ], Macro vipera vipers after emergence from their hibernac - lebetina (l iNNAEus , 1758) at birecik and ula. snakes were observed between 07:00 Şanlıurfa in southeastern Turkey, Aras am and 07:00 pm. shedding adult males Valley and Pafos on the island of Cyprus. in were identified visually by their thickened total, 54 specimens were seen, 15 of which tailbase and the presence of milky eyes and (eight specimens of Macrovipera and seven opaque skin. basic temporal (date, time of of Montivipera ) were identified as males in day) and geographical (latitude, longitude spring shedding and characterized by and elevation) information were recorded opaque (milky) eyes (Table 1). from each sampling site. The visited habi - The study area had a maximum latitu - tats were situated at elevations between 5 m dinal extension of 600 km in a north-south and 2,300 m a.s.l. Montivipera species were direction between records of Montivipera studied at the Turkish Aegean coast, and in wagneri (40°10’ N) and Macrovipera lebe- the western and central Taurus Massif [ M. tina (34°51’ N) and covered a longitudinal xanthina (GRAY , 1849) ], bolkar Mts. [ M. b. distance of 1,350 km from records of StuempelZinenkoMebert_Spring_activity_Montivipera-Macrovipera:HERPETOZOA.qxd 12.02.2019 15:04 Seite 4

128 N. s TüMPEl & o. Z iNENko & k. M EbERT

Table 1: Records of adult male vipers of the genera Macrovipera and Montivipera , including date and loca - tion of observation during their first spring ecdysis at the stage when the eyes turn visibly milky (opaque). Elevation in m a. s. l. Tab. 1: Fundortangaben zu den untersuchten adulten männlichen Vipern der Gattungen Macrovipera und Montivipera sowie Zeitpunkt während der ersten Frühjahrshäutung im stadium milchig-trüber Augen. seehöhe in m. ü. M.

species Number date Elevation locality Coordinates Art Anzahl datum seehöhe Fundort koordinaten Montivipera b. albizona 1 2011.V.17 1,850 Göksun 37°56’27.06”N / 36°31’49.00”E Montivipera b. bulgardaghica 1 2011.V.24 2,300 Arslanköy 37°02’45.82”N / 34°17’13.86”E Montivipera wagneri 1 2004.V.08 1,550 karakurt 34°17’13.86”N / 42°38’16.66”E Macrovipera l. lebetina 3 2013.iii.29 300 Cyprus 34°51’28.10”N / 32°25’40.17”E Macrovipera l. lebetina 1 2013.iii.29 20 Cyprus 34°49’19.98”N / 32°23’32.01”E Macrovipera l. euphratica 2 2015.iV.06 750 Şanlıurfa 37°13’20.92”N / 38°55’06.67”E Montivipera xanthina 2 2011.V.25 1,450 Gündoğmuş 36°51’29.87”N / 32°04’07.82”E Montivipera xanthina 2 2006.iV.15 280 selçuk 37°57’11.08”N / 27°29’07.67”E Macrovipera l. obtusa 2 2015.V.27 1,730 Günindi 40°13’20.36”N / 43°16’44.27”E

Montivipera xanthina in the west (27°28’ E) mally distributed population) for the date to Montivipera wagneri in the east (42°38’ values but not for the elevation values. E). data of all species, populations and There fore, the authors used the nonparamet - times were pooled due to the small sample ric spearman’s rho to test the correlation ( rs) size and because the phenomenon of spring between the variables date (in the form of shedding is known to be consistently pres - number of days following the first sighting) ent in all viper species in this study ( bRod - and elevation. MANN 1987 and the authors’ personal obser - statistical analyses were conducted vations) . on line using the software packages social statistical evaluation of the data in- science statistics ( sTANGRooM 2018 ) and cluded a check for normality using the sha - scistatCalc ( AHMEd 2013). The graph was piro-Wilk test. statistics rejected the null visualized using the software sTATisTiCA hypothesis (H 0 = data tested are from a nor - 6.0.

REsulTs ANd disCussioN

The data reveals the strong positive at 280 m a.s.l. during mid- correlation ( rs = 0.72, p < 0.01) between the April, whereas a population monitored at onset of spring shedding of male vipers and 1,450 m a.s.l. was still in hibernation at the the elevation of their record localities (Fig. beginning of April and courtship was 1). The significant ( p < 0.01) linear regres - observed at the end of May, 52 days later. sion (y = 29.6x +196.4; r2 = 0.85) indicates At the elevation of 2,300 m a.s.l., males of that the onset of spring shedding is tempo - Montivipera b. bulgardaghica reached the rally delayed with increasing elevation (m shedding state even later, at end of May. a.s.l.). For example, ecdysis of male it is widely known that geographical Macro vipera lebetina was observed at sea- location on a broad scale (latitude, longi - level on Cyprus at the end of March and at tude) are major determinants of temperature 1,730 m a.s.l. in northeastern Turkey in the conditions. in general it can be expected second half of May (ca. 40-50 days later). that these drivers put restrictions on life his - similarly, males of Montivipera xanthina tory and phenology of ectotherm , as were found in molting stage near the they have strong effects on seasonality, such StuempelZinenkoMebert_Spring_activity_Montivipera-Macrovipera:HERPETOZOA.qxd 12.02.2019 15:04 Seite 5

on elevation-related shifts of spring activity in Montivipera and Macrovipera 129

days / Tage ) . M

spearman correlation: .

ü rs = 0.72, p < 0.01

m (

e h ö h s

e 2

r y = 29.6x +196.4; r = 0.85 e e M

/

) . l . s . a

m (

n Montivipera o i t Macrovipera a v e l E

date / datum

Fig. 1: scatter plot showing temporal dependence between elevation of the record locality (m a.s.l.) and date of occurrence of milky-opaque eyes (developing 4-8 days prior to spring shedding) in mature male Montivipera (empty dots) and Macrovipera (filled dots) in Turkey and Cyprus. The statistical dependence is significant for the spearman rank correlation at the p < 0.01 level. Abb.1: Zeitliche Abhängigkeit des Auftretens der Augentrübung (4-8 Tage vor der Frühjahreshäutung) bei türkischen und zyprischen adulten männlichen Vipern der Gattungen Montivipera (leere kreise) und Macrovipera (gefüllte kreise) von der Höhenlage (m ü. M.) ihres Fundortes. der Zusammenhang ist für die spearman-Rangkorrelation auf dem Niveau p < 0,01 signifikant.

as timing of spring and duration of winter. conditions, e.g., temperatures and other en- sPERRY et al. (2010) analyzed the seasonal vironmental parameters. For the Common activity of the snake Pantherophis obsoletus Garter snake, Thamnophis sirtalis (liN- (s AY , 1823) across a latitudinal distance of NAEus , 1758), a temporal dissociation be - more than 1,500 km and associated temper - tween mating behavior (in spring), and ature data in North America. Even though gametogenesis and maximal sex steroid hor - the authors did not notice any variation in mone concentrations (in late summer) was activity throughout the study area, they reported ( CREWs 1984; C REWs et al. 1984). mentioned that ratsnakes in Texas did not in Macrovipera and Montivipera hibernate, whereas ratsnakes in both, illinois species, males produce mature sperm solely and ontario hibernated. in spring, which initiates their mating activ - Enhanced seasonality also affects re- ity after the first post hibernation shedding, productive functions such a mating, game - a process that is highly synchronized within togenesis or steroidogenesis, due to its cor - a population as in V. berus (NilsoN 1980). relation with cyclic fluctuations in climate Male spring-shedding is hormonally in- StuempelZinenkoMebert_Spring_activity_Montivipera-Macrovipera:HERPETOZOA.qxd 12.02.2019 15:04 Seite 6

130 N. s TüMPEl & o. Z iNENko & k. M EbERT

duced ( sAiNT GiRoNs & k RAMER 1963) and, ing season be gins up to two months earlier unlike the metabolically induced shedding, and snakes enter hibernation later. The ther - not connected to feeding rate and growth. mal regime in the mountains condenses vital Hence, spring-shedding can act as a bench - life history traits (reproduction, feeding) to mark within the reproductive cycle of these a six month time frame at most. male vipers. in summary, the present study com - However, topographic differences be- pares for the first time the onset of male tween lowland and alpine habitats in the spring shedding among different localities eastern Mediterranean have strong effects and species of eastern Mediterranean vipers on the temperature profiles comparative to and shows a delayed beginning of male those of latitudinal distances. The present activity by a later emergence from hiberna - study indicates that seasonal activity pat - tion with increase of elevation. Climate terns are not static within species and change will affect life history of reptiles and depend on the elevation of its habitat. populations may shift their active seasons to Annual surface activity is shorter in sub - earlier in the year. Further research is need - alpine Montivipera populations than at ed to generate a solid phenological data base coastal low elevation Macrovipera lebetina and to record how the activity of oriental or Montivipe ra xanthina in which the mat - vipers will be affected by climate change.

ACkNoWlEdGMENTs

The authors thank Volkswagen Nutzfahrzeuge logy, Aydın, TR), bayram GöçMEN , Mert kARiŞ (both Hannover for generous support of the fieldtrips in 2003 Ege university, İzmir, TR), as well as selami ToMRuk and 2004 and Volkswagen stiftung for funding the (Ecopark, Tekirova, TR) are acknowledged for compa - fieldtrip in 2011. benny TRAPP (Wuppertal, dE), Aziz ny and support in the field and ulrich JoGER AVCi and Emin boZkuRT (both Adnan Menderes uni- (staatliches Naturhistorisches Museum braunschweig, versity, Faculty of Art and science, department of bio- dE) for mentoring.

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dATE oF subMissioN: september 4, 2015 Corresponding editor: Andreas Maletzky

AuTHoRs: Nikolaus sTüMPEl (Corresponding author < [email protected] >) 1) , oleksandr ZiNENko 2) & konrad MEbERT 3) 1) staatliches Naturhistorisches Museum braunschweig, Gausstrasse 22, braunschweig, d-38106, Germany; 2) V.N. karazin kharkiv National university, svobody sq. 4, kharkiv 61058, ukraine; 3) institute of development, Ecology, Conservation and Cooperation, Via G. Tomasi di lampedusa 33, 00144 Rome, italy.